Rodent Empathy and Affective Neuroscience
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Neuroscience and Biobehavioral Reviews 35 (2011) 1864–1875 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review Rodent empathy and affective neuroscience Jules B. Panksepp ∗, Garet P. Lahvis ∗∗ Department of Behavioral Neuroscience, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, L470, Portland, OR 97239, USA article info abstract Article history: In the past few years, several experimental studies have suggested that empathy occurs in the social Received 11 October 2010 lives of rodents. Thus, rodent behavioral models can now be developed to elucidate the mechanistic Received in revised form 24 May 2011 substrates of empathy at levels that have heretofore been unavailable. For example, the finding that Accepted 27 May 2011 mice from certain inbred strains express behavioral and physiological responses to conspecific distress, while others do not, underscores that the genetic underpinnings of empathy are specifiable and that Keywords: they could be harnessed to develop new therapies for human psychosocial impairments. However, the Fear advent of rodent models of empathy is met at the outset with a number of theoretical and semantic Pain Distress problems that are similar to those previously confronted by studies of empathy in humans. The distinct Emotion underlying components of empathy must be differentiated from one another and from lay usage of the Social behavior term. The primary goal of this paper is to review a set of seminal studies that are directly relevant to Mus musculus developing a concept of empathy in rodents. We first consider some of the psychological phenomena Rattus Norvegicus that have been associated with empathy, and within this context, we consider the component processes, Reciprocity or endophenotypes of rodent empathy. We then review a series of recent experimental studies that Altruism demonstrate the capability of rodents to detect and respond to the affective state of their social partners. We focus primarily on experiments that examine how rodents share affective experiences of fear, but we also highlight how similar types of experimental paradigms can be utilized to evaluate the possibility that rodents share positive affective experiences. Taken together, these studies were inspired by Jaak Panksepp’s theory that all mammals are capable of felt affective experiences. © 2011 Elsevier Ltd. All rights reserved. Contents 1. Introduction ........................................................................................................................................ 1864 1.1. Empathy .................................................................................................................................... 1865 1.2. Foundational studies ....................................................................................................................... 1866 2. Social modulation of pain .......................................................................................................................... 1867 3. Social interaction with a recently distressed conspecific modulates subsequent learning about environmental signals that predict distress. 1867 4. Social transfer of fear .............................................................................................................................. 1869 5. Synopsis and conclusions .......................................................................................................................... 1871 References ......................................................................................................................................... 1873 1. Introduction writings of primatologist Franz de Waal, more principled and evo- lutionary based perspectives on empathy have emerged (de Waal, Historically, empathy has been considered a high-level affec- 2008). For instance, it is now generally accepted that many primate tive/cognitive process that is expressed exclusively by humans. species have a capacity for empathy, that empathy can be a proxi- However, recent scientific developments have placed this anthro- mate mechanism underlying the expression of altruistic behavior, pocentric view into question. Prompted in part by the research and and that empathy is the product of an integrated set of brain pro- cesses. Moreover, contemporary views of empathy consider its expression to be a product of several behavioral, affective and cog- ∗ nitive processes, each of which can vary with development, context Corresponding author. Tel.: +1 503 494 8286; fax: +1 503 494 6877. ∗∗ and species (see below). Deconstructing empathy into specifiable Corresponding author. Tel.: +1 503 346 0820; fax: +1 503 494 6877. E-mail addresses: [email protected] (J.B. Panksepp), [email protected] components is useful elucidating the biological substrates that con- (G.P. Lahvis). tribute to impairments in social interaction. 0149-7634/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2011.05.013 J.B. Panksepp, G.P. Lahvis / Neuroscience and Biobehavioral Reviews 35 (2011) 1864–1875 1865 In this paper, we consider one core feature of empathy in rodents response, which allowed individuals to relate with the emotional – the ability to share affective experiences. We review and compare state of others even though they did not necessarily share the same the experimental approaches and results of a series of recent papers state (for an excellent review of different definitions of empathy that explored different aspects of rodent behavior in response to the and its historical evolution see Davis, 1994). distress of conspecifics. Rather than reviewing research on empathy Theoretical developments in empathy research now view the in primates (Davis, 1994; Farrow and Woodruff, 2007; Silk, 2007; expression of empathy as the result of an interaction between sev- Decety, 2010), we examine how shared affect can be modeled in eral component processes, both affective and cognitive (Hoffman, laboratory rats and mice. In this regard, studies of shared affect in 1987; Preston and de Waal, 2002; Decety and Jackson, 2004). rodents can provide a level of biological resolution that has never Preston and de Waal (2002) hypothesized that these processes uti- been achieved in empathy research. lize an ancient perception–action coupling mechanism in which a Several of the studies that we describe employ a fear- subject’s attention to the ‘state’ of another can automatically acti- conditioning paradigm in which an individual is challenged to learn vate the same state in the subject. Regardless of the underlying an association between a conditioned stimulus (CS), such as a tone mechanism, this model serves as a very useful heuristic insofar or context, and an unconditioned stimulus (UCS), such as a deliv- that viewing empathy as a psychological phenomenon which stems ery of a shock. In a standard fear-conditioning paradigm, a subject from several underlying processes offers a practical strategy for learns to associate the CS with a UCS that engenders pain. However, employing biological approaches in empathy research. In the rest many of the studies described herein utilize a very different UCS, of this section, we review what some of these component pro- a distress cue that has been generated by the induction of pain in cesses are in attempt to clarify our own hypothesis that rodents another individual (Section 4). Consistent with the affective neuro- are capable of sharing affective experiences. science approach (Panksepp, 1998), we adopt the perspective that Emotional contagion is a psychological process that is relevant such associations can be learned because changes in an animal’s to empathy and refers to a phenomenon in which the perception of subjective state occur while others are undergoing distress. In this a behavioral change in an individual appears to automatically acti- scenario, a subject’s subsequent responsiveness to a CS thus reflects vate the same process in another individual. Emotional contagion its previous emotional experiences with a conspecific in pain. is thus a reflexive behavioral process among individuals within the A basic premise of affective neuroscience is that careful behav- context of a motivationally salient event. By definition, contagion ioral and neuroanatomical manipulations in the laboratory can requires that two individuals contemporaneously express a behav- yield insights into how affective and cognitive processes are dis- ior that reflects a common experience. Perhaps the most common tinct both in terms of their overt expression and their respective examples of emotional contagion in humans are infectious crying neural circuitries (Panksepp, 2005). Through the lens of affective among babies and yawning among adults. Although emotional con- neuroscience, we can envision building a robust framework for tagion fits within a more generally accepted definition of empathy; elucidating the neurobiological substrates that underlie different “the generation of an affective state more appropriate to the sit- aspects of empathy in animals. uation of another compared to one’s own” (Hoffman, 1975), it is excluded from others, particularly when there is an emphasis on 1.1. Empathy the ability to distinguish self from other. Importantly, emotional contagion does not require an ability to discern whether the source The study of empathy is heavily influenced by questions about of an affective experience comes from one’s